Research Article: Infection of Plasmodiophora brassicae changes the fungal endophyte community of tumourous stem mustard roots as revealed by high-throughput sequencing and culture-dependent methods

Date Published: June 12, 2019

Publisher: Public Library of Science

Author(s): Xueliang Tian, Diandong Wang, Zhenchuan Mao, Limei Pan, Jingjing Liao, Zhaoming Cai, Cheng Gao.

http://doi.org/10.1371/journal.pone.0214975

Abstract

Diverse fungal endophytes live in plants and are shaped by some abiotic and biotic stresses. Plant disease as particular biotic stress possibly gives an impact on the communities of fungal endophytes. In this study, clubroot disease caused by an obligate biotroph protist, Plasmodiophora brassicae, was considered to analyze its influence on the fungal endophyte community using an internal transcribed spacer (ITS) through high-throughput sequencing and culture-dependent methods. The results showed that the diversity of the endophyte community in the healthy roots was much higher than the clubroots. Ascomycota was the dominant group of endophytes (Phoma, Mortierella, Penicillium, etc.) in the healthy roots while P. brassicae was the dominant taxon in the clubroots. Hierarchical clustering, principal component analysis (PCA), principal coordinates analysis (PCoA) and analysis of similarities (ANOSIM) indicated significant differences between the endophyte communities in the healthy roots and clubroots. Linear discriminant analysis effect size (LefSe) analysis showed that the dominant genera could be regarded as potential biomarkers. The endophyte community in the healthy roots had a more complex network compared with the clubroots. Also, many plant pathogenic Fusarium were isolated from the clubroots by the culture-dependent method. The outcome of this study illustrates that P. brassicae infection may change the fungal endophyte community associated with the roots of tumourous stem mustard and facilitates the entry of soil pathogen into the roots.

Partial Text

Fungal endophytes have a close relationship with the host plants and they live in their tissues [1,2]. They provide many ecological and physiological advantages to their hosts, such as growth promotion [3], resistance to plant pathogens and adaptability to various abiotic stresses such as temperature, pH, and osmotic pressure as well as biotic stresses [4–6]. Similarly, the fungal endophyte communities are also affected by abiotic and biotic stresses [7]. Plant disease as particular biotic stress results in significant changes in the physiology of the plant. These changes and pathogen itself may affect the diversity and composition of the fungal endophyte inhabiting the plant tissues and their interactions with their host plant [8–10].

In this study, a high diversity of fungal endophyte in the healthy roots of tumourous stem mustard has been found out using high-throughput sequencing. Our results agree with the early reports that the plants can harbor a diversity of endophytic fungi in their healthy tissues, especially in the root system which is considered to be the most suitable habitat for endophytic fungi [27,28]. Ascomycota is reported to be the most common group of endophytic fungi [29], suggesting that they are suitable for the ecological niche of plant tissue. Zhao also reported Ascomycota as the dominant group of endophytic fungi in the roots of oilseed rape (Brassica napus) [17]. Also in this study, Ascomycota is the dominant taxon in the healthy roots of tumourous stem mustard. In the phylum Ascomycota, Phoma, Mortierella, Penicillium, and Fusarium were the common fungal genera in the healthy roots of tumourous stem mustard. Arie et al. reported that Phoma glomerata produces epoxydon and inhibits clubroot disease, demonstrating that Phoma in the healthy roots of tumourous stem mustard may accomplish a similar function [30,31]. Mortierella was also detected in the roots of oilseed rape using high-throughput sequencing [17]. Melo et al. confirmed that the endophytic M. alpina in the moss Schistidium antarctici produces antibiotics, antioxidants, and polyunsaturated fatty acids, which improve the environmental suitability of the plant host [32]. Wani et al. also found that endophytic M. alpina promotes the biosynthesis of Crocus apocarotenoid and enhances environmental stress tolerance [33]. These results reflect that the endophytic Mortierella is a benefit to the plant, which indicates that Mortierella in tumourous stem mustard is beneficial to the host. Marinho et al. and Lin et al. both reported that endophytic Penicillium produces active polyketides [34,35], reflecting that Penicillium in tumourous stem mustard may produce similar substances.

In conclusion, the obtained data from this study showed that the fungal endophyte community in the clubroots are markedly different from the healthy roots in terms of alpha and beta diversity, suggesting that the infection of P. brassicae changes the fungal endophyte community in tumourous stem mustard roots. Future work should involve identifying the pathogenicity of F. oxysporum and F. solani on tumourous stem mustard. Moreover, in the evaluation some endophytic fungi with biocontrol activity against P. brassicae could also be considered in the evaluation.

 

Source:

http://doi.org/10.1371/journal.pone.0214975

 

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